Mechanistic consequences of hnRNP C binding to both RNA termini of poliovirus negative-strand RNA intermediates

Journal of Virology

Volumn 84, Issue 9, 2010, Pages 4229-4242

  Ertel, Kenneth J ^a,b   Brunner, Jo Ellen ^a   Semler, Bert L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN C; RIBONUCLEOPROTEIN; VIRUS RNA;

3' UNTRANSLATED REGION; ARTICLE; HELA CELL; IN VITRO STUDY; NONHUMAN; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA REPLICATION; RNA SEQUENCE; RNA SYNTHESIS; VIROGENESIS; VIRUS INFECTION; VIRUS REPLICATION;

3' UNTRANSLATED REGIONS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP C; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; POLIOVIRUS; PROTEIN BINDING; RNA, VIRAL; SEQUENCE DELETION; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

POLIOVIRUS;

EID: 77950851941     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02198-09     Document Type: Article

References (59)

1. Aldabe, R., and L. Carrasco. 1995. Induction of membrane proliferation by poliovirus proteins 2C and 2BC. Biochem. Biophys. Res. Commun. 206:64-76.
2. Banerjee, R., A. Echeverri, and A. Dasgupta. 1997. Poliovirus-encoded 2C polypeptide specifically binds to the 3′-terminal sequences of viral negative-strand RNA. J. Virol. 71:9570-9578. (Pubitemid 27492404)
3. Banerjee, R., W. Tsai, W. Kim, and A. Dasgupta. 2001. Interaction of poliovirus-encoded 2C/2BC polypeptides with the 3′ terminus negative-strand cloverleaf requires an intact stem-loop b. Virology 280:41-51. (Pubitemid 34158050)
4. Barton, D. J., and J. B. Flanegan. 1997. Synchronous replication of poliovirus RNA: initiation of negative-strand RNA synthesis requires the guanidine-inhibited activity of protein 2C. J. Virol. 71:8482-8489.
5. Barton, D. J., B. J. O'Donnell, and J. B. Flanegan. 2001. 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J. 20:1439-1448. (Pubitemid 32233983)
6. Bartz, S. R., and M. A. Vodicka. 1997. Production of high-titer human immunodeficiency virus type 1 pseudotyped with vesicular stomatitis virus glycoprotein. Methods 12:337-342.
7. Bedard, K. M., B. L. Walter, and B. L. Semler. 2004. Multimerization of poly(rC) binding protein 2 is required for translation initiation mediated by a viral IRES. RNA 10:1266-1276.
8. Belov, G. A., A. G. Evstafieva, Y. P. Rubtsov, O. V. Mikitas, A. B. Vartapetian, and V. I. Agol. 2000. Early alteration of nucleocytoplasmic traffic induced by some RNA viruses. Virology 275:244-248.
9. Belov, G. A., C. Habbersett, D. Franco, and E. Ehrenfeld. 2007. Activation of cellular Arf GTPases by poliovirus protein 3CD correlates with virus replication. J. Virol. 81:9259-9267.
10. Blyn, L. B., K. M. Swiderek, O. Richards, D. C. Stahl, B. L. Semler, and E. Ehrenfeld. 1996. Poly(rC) binding protein 2 binds to stem-loop IV of the poliovirus RNA 5′ noncoding region: identification by automated liquid chromatography-tandem mass spectrometry. Proc. Natl. Acad. Sci. U. S. A. 93:11115-11120.
11. Blyn, L. B., J. S. Towner, B. L. Semler, and E. Ehrenfeld. 1997. Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J. Virol. 71:6243-6246.
12. Brown, D. M., C. T. Cornell, G. P. Tran, J. H. Nguyen, and B. L. Semler. 2005. An authentic 3′ noncoding region is necessary for efficient poliovirus replication. J. Virol. 79:11962-11973.
13. Brown, D. M., S. E. Kauder, C. T. Cornell, G. M. Jang, V. R. Racaniello, and B. L. Semler. 2004. Cell-dependent role for the poliovirus 3′ noncoding region in positive-strand RNA synthesis. J. Virol. 78:1344-1351.
14. Brunner, J. E., K. J. Ertel, J. M. Rozovics, and B. L. Semler. 26 February 2010. Delayed kinetics of poliovirus RNA synthesis in a human cell line with reduced levels of hnRNP C proteins. Virology [Epub ahead of print.]
15. Brunner, J. E., J. H. C. Nguyen, H. H. Roehl, T. V. Ho, K. M. Swiderek, and B. L. Semler. 2005. Functional interaction of heterogeneous nuclear ribonucleoprotein C with poliovirus RNA synthesis initiation complexes. J. Virol. 79:3254-3266.
16. Cho, M. W., N. Teterina, D. Egger, K. Bienz, and E. Ehrenfeld. 1994. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology 202:129-145.
17. Choi, K. S., A. Mizutani, and M. C. Lai. 2004. SYNCRIP, a member of the heterogeneous nuclear ribonucleoprotein family, is involved in mouse hepatitis virus RNA synthesis. J. Virol. 78:13153-13162.
18. Cui, T., S. Sankar, and A. G. Porter. 1993. Binding of encephalomyocarditis virus RNA polymerase to the 3′-noncoding region of the viral RNA is specific and requires the 3′-poly(A) tail. J. Biol. Chem. 268:26093-26098.
19. Gamarnik, A. V., and R. Andino. 1997. Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3:882-892. (Pubitemid 27332738)
20. Gamarnik, A. V., and R. Andino. 2000. Interactions of viral protein 3CD and poly(rC) binding protein with the 5′ untranslated region of the poliovirus genome. J. Virol. 74:2219-2226. (Pubitemid 30091476)
21. Giachetti, C., and B. L. Semler. 1991. Role of a viral membrane polypeptide in strand-specific initiation of poliovirus RNA synthesis. J. Virol. 65:2647-2654.
22. Gorlach, M., M. Wittekind, R. A. Beckman, L. Mueller, and G. Dreyfuss. 1992. Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J. 11:3289-3295.
23. Gustin, K. E., and P. Sarnow. 2001. Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J. 20:240-249.
24. Gustin, K. E., and P. Sarnow. 2002. Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J. Virol. 76:8787-8796.
25. Haller, A. A., and B. L. Semler. 1992. Linker scanning mutagenesis of the internal ribosome entry site of poliovirus RNA. J. Virol. 66:5075-5086.
26. Harris, K. S., W. Xiang, L. Alexander, W. S. Lane, A. V. Paul, and E. Wimmer. 1994. Interaction of poliovirus polypeptide 3CDpro with the 5′ and 3′ termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding. J. Biol. Chem. 269:27004-27014.
27. Herold, J., and R. Andino. 2000. Poliovirus requires a precise 5′ end for efficient positive-strand RNA synthesis. J. Virol. 74:6394-6400. (Pubitemid 30429805)
28. Herold, J., and R. Andino. 2001. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell 7:581-591. (Pubitemid 32706350)
29. Holcik, M., B. W. Gordon, and R. G. Korneluk. 2003. The internal ribosome entry site-mediated translation of antiapoptotic protein XIAP is modulated by the heterogeneous nuclear ribonucleoproteins C1 and C2. Mol. Cell. Biol. 23:280-288.
30. Leong, L. E. C., C. T. Cornell, and B. L. Semler. 2002. Processing determinants and functions of cleavage products of picornavirus polyproteins, p. 187-197. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
31. Lescrinier, E. M., M. Tessari, F. J. Van Kuppeveld, W. J. Melchers, C. W. Hilbers, and H. A. Heus. 2003. Structure of the pyrimidine-rich internal loop in the poliovirus 3′-UTR: the importance of maintaining pseudo-2-fold symmetry in RNA helices containing two adjacent non-canonical base-pairs. J. Mol. Biol. 331:759-769.
32. McBride, A. E., A. Schlegel, and K. Kirkegaard. 1996. Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells. Proc. Natl. Acad. Sci. U. S. A. 93:2296-2301.
33. Molla, A., A. V. Paul, and E. Wimmer. 1991. Cell-free, de novo synthesis of poliovirus. Science 254:1647-1651.
34. Myslinski, E., J. C. Ame, A. Krol, and P. Carbon. 2001. An unusually compact external promoter for RNA polymerase III transcription of the human H1RNA gene. Nucleic Acids Res. 29:2502-2509. (Pubitemid 32600305)
35. Nakielny, S., and G. Dreyfuss. 1996. The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals. J. Cell Biol. 134:1365-1373. (Pubitemid 26318011)
36. Novak, J. E., and K. Kirkegaard. 1991. Improved method for detecting poliovirus negative strands used to demonstrate specificity of positive-strand encapsidation and the ratio of positive to negative strands in infected cells. J. Virol. 65:3384-3387.
37. Parsley, T. B., J. S. Towner, L. B. Blyn, E. Ehrenfeld, and B. L. Semler. 1997. Poly(rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA 3:1124-1134. (Pubitemid 27424279)
38. Paul, A. V. 2002. Possible unifying mechanism of picornavirus genome replication, p. 227-246. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
39. Perera, R., S. Daijogo, B. L. Walter, J. H. C. Nguyen, and B. L. Semler. 2007. Cellular protein modification by poliovirus: the two faces of poly(rC)-binding protein. J. Virol. 81:8919-8932. (Pubitemid 47311436)
40. Pilipenko, E. V., K. Poperechny, S. V. Maslova, W. J. G. Melchers, H. J. Bruins Slot, and V. I. Agol. 1996. Cis-element, oriR, involved in the initiation of (-) strand poliovirus RNA: a quasi-globular multi-domain RNA structure maintained by tertiary ('kissing') interactions. EMBO J. 15:5428-5436.
41. Roehl, H. H., T. B. Parsley, T. V. Ho, and B. L. Semler. 1997. Processing of a cellular polypeptide by 3CD proteinase is required for poliovirus ribonucleoprotein complex formation. J. Virol. 71:578-585.
42. Roehl, H. H., and B. L. Semler. 1994. In vitro biochemical methods for investigating RNA-protein interactions in picornaviruses, p. 169-182. In K. W. Adolph (ed.), Methods in molecular genetics, vol.4. Academic Press, Orlando, FL.
43. Roehl, H. H., and B. L. Semler. 1995. Poliovirus infection enhances the formation of two ribonucleoprotein complexes at the 3′ end of viral negative-strand RNA. J. Virol. 69:2954-2961.
44. Saiz, M., S. Gomez, E. Martinez-Salas, and F. Sobrino. 2001. Deletion or substitution of the aphthovirus 3′ NCR abrogates infectivity and virus replication. J. Gen. Virol. 82:93-101.
45. Scott, W. G., J. B. Murray, J. R. Arnold, B. L. Stoddard, and A. Klug. 1996. Capturing the structure of a catalytic RNA intermediate: the hammerhead ribozyme. Science 274:2065-2069.
46. Swanson, M. S., and G. Dreyfuss. 1988. RNA binding specificity of hnRNP proteins: a subset bind to the 3′ end of introns. EMBO J. 7:3519-3529.
47. Swift, S., J. Lorens, P. Achacoso, and G. P. Nolan. 2001. Rapid production of retroviruses for efficient gene delivery to mammalian cells using 293T cell-based systems. Curr. Protoc. Immunol. 31:10.17.14-10.17.29.
48. Todd, S., J. H. Nguyen, and B. L. Semler. 1995. RNA-protein interactions directed by the 3′ end of human rhinovirus genomic RNA. J. Virol. 69:3605-3614.
49. Todd, S., and B. L. Semler. 1996. Structure-infectivity analysis of the human rhinovirus genomic RNA 3′ non-coding region. Nucleic Acids Res. 24:2133-2142. (Pubitemid 26174557)
50. Todd, S., J. S. Towner, D. M. Brown, and B. L. Semler. 1997. Replication-competent picornaviruses with complete genomic RNA 3′ noncoding region deletions. J. Virol. 71:8868-8874. (Pubitemid 27446474)
51. Tuteja, R., and N. Tuteja. 1998. Nucleolin: a multifunctional major nucleolar phosphoprotein. Crit. Rev. Biochem. Mol. Biol. 33:407-436.
52. van Ooij, M. J., C. Polacek, D. H. Glaudemans, J. Kuijpers, F. J. Van Kuppeveld, R. Andino, V. I. Agol, and W. J. Melchers. 2006. Polyadenylation of genomic RNA and initiation of antigenomic RNA in a positive-strand RNA virus are controlled by the same cis-element. Nucleic Acids Res. 34:2953-2965.
53. Waggoner, S., and P. Sarnow. 1998. Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells. J. Virol. 72:6699-6709. (Pubitemid 28323988)
54. Walter, B. L., J. H. Nguyen, E. Ehrenfeld, and B. L. Semler. 1999. Differential utilization of poly(rC) binding protein 2 in translation directed by picornavirus IRES elements. RNA 5:1570-1585.
55. Walter, B. L., T. B. Parsley, E. Ehrenfeld, and B. L. Semler. 2002. Distinct poly(rC) binding protein KH domain determinants for poliovirus translation initiation and viral RNA replication. J. Virol. 76:12008-12022.
56. Wan, L., J. K. Kim, V. W. Pollard, and G. Dreyfuss. 2001. Mutational definition of RNA-binding and protein-protein interaction domains of heterogeneous nuclear RNP C1. J. Biol. Chem. 276:7681-7688.
57. Waterhouse, N., S. Kumar, Q. Song, P. Strike, L. Sparrow, G. Dreyfuss, E. S. Alnemri, G. Litwack, M. Lavin, and D. Watters. 1996. Heteronuclear ribonucleoproteins C1 and C2, components of the spliceosome, are specific targets of interleukin 1 beta-converting enzyme-like proteases in apoptosis. J. Biol. Chem. 271:29335-29341.
58. Yang, Y., R. Rijnbrand, S. Watowich, and S. M. Lemon. 2003. Genetic evidence for an interaction between a picornaviral cis-acting RNA replication element and 3CD protein. J. Biol. Chem. 279:12659-12667.
59. Zuker, M., D. H. Mathews, and D. H. Turner. 1999. Algorithms and thermodynamics for RNA secondary structure prediction: a practical guide, p. 11-43. In J. Barciszewski and B. F. C. Clark (ed.), RNA biochemistry and biotechnology. NATO Science Series, vol.70. Kluwer Academic Publishers, Boston, MA. (Pubitemid 29248642)